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The Ecology of Acidobacteria: Moving Beyond Genes and Genomes fmicb-07-00744 May 27, 2016 Time: 15:45 # 1 REVIEW published: 31 May 2016 doi: 10.3389/fmicb.2016.00744 The Ecology of Acidobacteria: Moving beyond Genes and Genomes Anna M. Kielak1†, Cristine C. Barreto2†, George A. Kowalchuk3, Johannes A. van Veen1 and Eiko E. Kuramae1* 1 Department of Microbial Ecology, The Netherlands Institute of Ecology – Koninklijke Nederlandse Akademie van Wetenschappen, Wageningen, Netherlands, 2 Graduate Program in Genomic Sciences and Biotechnology, Universidade Católica de Brasília, Brasília, Brazil, 3 Ecology and Biodiversity Group, University of Utrecht, Utrecht, Netherlands The phylum Acidobacteria is one of the most widespread and abundant on the planet, yet remarkably our knowledge of the role of these diverse organisms in the functioning of terrestrial ecosystems remains surprisingly rudimentary. This blatant knowledge gap stems to a large degree from the difficulties associated with the cultivation of these bacteria by classical means. Given the phylogenetic breadth of the Acidobacteria, which is similar to the metabolically diverse Proteobacteria, it is clear that detailed and functional descriptions of acidobacterial assemblages are necessary. Fortunately, recent advances are providing a glimpse into the ecology of members of the phylum Acidobacteria. These include novel cultivation and enrichment strategies, genomic Edited by: characterization and analyses of metagenomic DNA from environmental samples. Here, Rich Boden, we couple the data from these complementary approaches for a better understanding University of Plymouth, UK of their role in the environment, thereby providing some initial insights into the ecology of Reviewed by: Stephanie A. Eichorst, this important phylum. All cultured acidobacterial type species are heterotrophic, and University of Vienna, Austria members of subdivisions 1, 3, and 4 appear to be more versatile in carbohydrate Hinsby Cadillo-Quiroz, utilization. Genomic and metagenomic data predict a number of ecologically relevant Arizona State University, USA capabilities for some acidobacteria, including the ability to: use of nitrite as N source, *Correspondence: Eiko E. Kuramae respond to soil macro-, micro nutrients and soil acidity, express multiple active [email protected] transporters, degrade gellan gum and produce exopolysaccharide (EPS). Although †These authors have contributed these predicted properties allude to a competitive life style in soil, only very few of these equally to this work. prediction shave been confirmed via physiological studies. The increased availability of Specialty section: genomic and physiological information, coupled to distribution data in field surveys and This article was submitted to experiments, should direct future progress in unraveling the ecology of this important Terrestrial Microbiology, a section of the journal but still enigmatic phylum. Frontiers in Microbiology Keywords: Acidobacteria, carbohydrate metabolism, transporters, nitrogen metabolism, EPS, soil factors Received: 08 October 2015 Accepted: 03 May 2016 Published: 31 May 2016 INTRODUCTION Citation: Kielak AM, Barreto CC, Although the Acidobacteria were only recognized as a phylum relatively recently, their abundance Kowalchuk GA, van Veen JA across a range of ecosystems, especially soils, has demanded research into their ecology. 16S rRNA and Kuramae EE (2016) The Ecology gene-based approaches as well as environmental shotgun metagenomic analyses have revealed of Acidobacteria: Moving beyond Genes and Genomes. that the Acidobacteria represent a highly diverse phylum resident to a wide range of habitats Front. Microbiol. 7:744. around the globe (Chow et al., 2002; Kuske et al., 2002; Gremion et al., 2003; Quaiser et al., 2003; doi: 10.3389/fmicb.2016.00744 Fierer et al., 2005; Stafford et al., 2005; Janssen, 2006; Sanguin et al., 2006; de Carcer et al., 2007; Frontiers in Microbiology | www.frontiersin.org 1 May 2016 | Volume 7 | Article 744 fmicb-07-00744 May 27, 2016 Time: 15:45 # 2 Kielak et al. Ecology of Acidobacteria Kim et al., 2007; Singh et al., 2007; DeAngelis et al., 2009; Jesus Acidobacteria phylum. Based on phylogenetic analysis of 16S et al., 2009; Kielak et al., 2009; Navarrete et al., 2010, 2013b; Zhang rRNA gene sequences, the Acidobacteria phylum raised from et al., 2014). However, despite their high abundance and diversity, the originally described four to six subdivisions (Kuske et al., we still have relatively little information regarding the actual 1997; Ludwig et al., 1997; Barns et al., 1999, 2007) to over eight activities and ecology of members of this phylum, a shortcoming subdivisions in 1998 (Hugenholtz et al., 1998) and in 2005 that can be attributed to a large extent to the difficulties in this number increased to 11 (Zimmermann et al., 2005) deeply cultivating the majority of acidobacteria and their poor coverage branching and strongly supported subdivisions. Currently there in bacterial culture collections (Bryant et al., 2007; Lee et al., 2008; are 26 accepted subdivisions (Barns et al., 2007) in the Ribosomal da Rocha et al., 2009; Eichorst et al., 2011; Navarrete et al., 2013b). Database Project. The first recognized strain and species of the However, environmental surveys have provided insight into some phylum Acidobacteria was Acidobacterium capsulatum obtained the environmental factors that may drive acidobacteria dynamics, from an acid mine drainage in Japan (Kishimoto and Tano, such as pH and nutrients (Fierer et al., 2007; Jones et al., 2009; 1987; Kishimoto et al., 1991; Abed et al., 2002). Although the Lauber et al., 2009; Navarrete et al., 2013b). second isolate belonging to this phylum was Holophaga foetida In 2009, the first sequenced genomes of acidobacteria strains first described in 1994, it was not initially recognized as related became available, providing preliminary genetic insights into to Acidobacteria capsulatum. Instead, it was thought to belong the potential physiology and environment functions of several to the phylum Proteobacteria (Liesack et al., 1994). A few years members of this phylum (Ward et al., 2009). In these first later, a closely related bacterium named Geothrix fermentans genomic studies, five aspects of physiological received particular was isolated (Coates et al., 1999) and subsequently another attention: (i) carbon usage, (ii) nitrogen assimilation, (iii) closely related bacterium Acanthopleuribacter pedis, the first metabolism of iron, (iv) antimicrobials, and (v) abundance acidobacteria obtained from a marine sample, was described of transporters. Besides genome sequencing of cultivated (Fukunaga et al., 2008). Since these isolates were very distantly isolates, addition information regarding genomic properties of related to A. capsulatum, it was proposed that it should be acidobacteria has been derived from metagenomics studies (Liles included in a new class named Holophagae. Acidobacteriia et al., 2003; Quaiser et al., 2003, 2008; Riaz et al., 2008; Jones et al., and Holophagae are the only classes currently included in the 2009; Kielak et al., 2010; Parsley et al., 2011; Faoro et al., 2012; most recent edition of the Bergey’s Manual (Thrash and Coates, Navarrete et al., 2013b; Mendes et al., 2014). 2014). In this review, we couple the complementary data coming Currently Acidobacteria phylum has 26 subdivisions based from physiological, genomic and metagenomics studies to seek on the extremely broad diversity of acidobacterial populations a better understanding of the role of Acidobacteria in the found in uranium-contaminated soils (Barns et al., 2007). Newly environment, thereby providing some initial insights into the characterized acidobacteria from subdivision 1 may challenge ecology of this important phylum. We aim to not only give a more this taxonomy in the near future, since of 16S rRNA gene analysis complete picture of the current knowledge of Acidobacteria, but has consistently shown that the genera Acidobacteria,‘Acidipila’ also seek to provide a solid base for future experiments geared (Okamura et al., 2011), Telmatobacter (Pankratov et al., 2012), toward gaining a better understanding of the ecological roles and Acidicapsa (Kulichevskaya et al., 2012) form a group that is played by members of this phylum. distinct from the genera Granulicella, Terriglobus, Bryocella, and Edaphobacter (Eichorst et al., 2007; Koch et al., 2008; Pankratov and Dedysh, 2010; Männistö et al., 2011, 2012; Rawat et al., HISTORY AND GENERAL INFORMATION 2012a,b; Baik et al., 2013; Whang et al., 2014). ON THE PHYLUM Acidobacteria The vast majority of isolates cultivated to date are affiliated with acidobacteria subdivision 1 (Class Acidobacteriia). They are The introduction of molecular biological strategies into microbial all heterotrophic, most species are aerobic or microaerophilic ecology over the past decades has yielded a new perspective on and some species (Telmatobacter bradus, Acidobacterium the breadth and vastness of microbial diversity. The phylum capsulatum) are facultative anaerobic bacteria (Pankratov of the Acidobacteria is one of the bacterial lineages that has et al., 2012). Members of subdivisions 3, 4, 8 (currently profited most from the cultivation-independent interrogation Class Holophagae), 10, and 23 are heterotrophic as well. of environmental samples. Indeed, in the past two decades, Thermotomaculum (subdivision 10) and Thermoanaerobaculum this phylum has grown from being virtually unknown to being (subdivision 23) are thermophilic anaerobic bacteria (Izumi et al., recognized
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